Download Parasitism, predation and the evolution of animal personalities

Ecology Letters, (2010) 13: 1449–1458
IDEA AND
PERSPECTIVE
1
Parasitism, predation and the evolution of animal
personalities
2
Raine Kortet, * Ann V. Hedrick
and Anssi Vainikka3
1
Department of Biology,
University of Eastern Finland,
P.O. Box 111, FI 80101 Joensuu,
Finland
2
Department of Neurobiology,
Physiology & Behavior and
Animal Behavior Graduate
Group, Division of Biological
Sciences, One Shields Avenue,
University of California, Davis,
CA 95616, USA
3
Department of Biology,
doi: 10.1111/j.1461-0248.2010.01536.x
Abstract
Trade-offs between behavioural traits promoting high life-history productivity and
mortality may fuel the evolution of animal personalities. We propose that parasites,
including pathogens, impose fitness costs comparable to those from predators, and
influence the adaptiveness of personality traits associated with productivity (PAPs).
Whether personality traits are adaptive or not may also depend on individual
immunological capacity. We illustrate this using a conceptual example in which the
optimal level of PAPs depends on predation, parasitism and host compensation
(resistance and tolerance) of parasitismÕs negative effects. We assert that inherent
differences in host immune function can produce positive feedback loops between
resource intake and compensation of parasitismÕs costs, thereby providing variation
underlying the evolution of stable personalities. Our approach acknowledges the
condition dependence of immune function and co-evolutionary dynamics between hosts
and parasites.
University of Oulu, P.O. Box
3000, FI 90014 University of
Oulu, Finland
*Correspondence: E-mail:
[email protected]
Keywords
Behavioural syndrome, feedback loop, growth-mortality trade-off, parasitism, pathogen,
personality.
Ecology Letters (2010) 13: 1449–1458
INTRODUCTION
Observations on consistent, individually characteristic
behaviours across a wide variety of taxa have motivated
enormous interest in animal personalities and their evolutionary importance (reviewed by Dall et al. 2004; Sih et al.
2004; Dingemanse & Réale 2005; Bell 2007; Réale et al.
2007; Biro & Stamps 2008; Stamps and Groothuis 2010).
Even though animal personalities can sometimes appear
maladaptive in contrast to fully flexible context-dependent
behaviour, their possible adaptive significance is becoming
evident (Sih & Bell 2008; Dingemanse et al. 2010; Luttbeg &
Sih 2010). In this article, we define (animal) ÔpersonalityÕ
(also known as ÔtemperamentÕ or Ôcoping styleÕ) as behaviour
that varies among individuals, but is consistent across time
and ⁄ or contexts within individuals (Stamps and Groothuis
2010). For example, animals with a ÔshyÕ personality are
consistently cautious and avoid risk taking, whereas those
with a ÔboldÕ personality are consistently incautious and
prone to take risks (Sih et al. 2004).
Predation is generally considered the major cause of
mortality for ÔboldÕ, risk-taking individuals (e.g. Smith &
Blumstein 2008; Biro & Booth 2009), and thus has been
identified as an important factor in the evolution of
personality traits, such as activity, exploration and boldness
(e.g. Dingemanse et al. 2007). Predation incurs not only
direct mortality costs, but also the loss of resources via
intimidation effects (Preisser et al. 2005; Stamps 2007).
Consequently, the adaptive significance of risk taking
depends on the relative costs and benefits of being bold
at different times and in different microenvironments: bold
individuals obtain a fitness advantage (higher resourceintake rates), if predation risk is low, whereas shy individuals
can have higher fitness, if predation risk is high (Sih et al.
2004). As the fitness costs of risk taking may increase in
parallel with the fitness benefits accompanying increased
resource-intake rates, individuals with different levels of
boldness may, on average, achieve equal lifetime fitness and
a continuum of individuals from shy to bold will remain in a
population (Stamps 2007; Biro & Stamps 2008).
Although predation is widely recognized as an important
agent in the evolution of personality, the potential effect of
parasitism on the evolution of animal personalities has been
largely ignored. Nonetheless, parasitism imposes fitness
costs comparable to those of predation (Raffel et al. 2008;
Rohr et al. 2009; Schmid-Hempel 2009), as parasites
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1450 R. Kortet, A. V. Hedrick and A. Vainikka
(including microparasites and pathogens such as viruses and
bacteria) are significant sources of mortality and sublethal
fitness costs. Very recently, Barber and Dingemanse (2010)
outlined the potential importance of parasites in the
evolution of animal personality. Here, in accordance with
Barber and Dingemanse (2010), we argue that because
parasites have major impacts on fitness (including behavioural components of fitness), and because certain personality
traits can affect the probability of acquiring and resisting
parasites (Lozano 1991; Wilson et al. 1993; Hart 1997),
parasites should influence the evolution of personality.
We also discuss the implications of this for recent models
for the evolution of personality, and explain why parasitism
should help generate and maintain consistent interindividual
variation in behaviour.
Growth-mortality trade-offs, and feedback loops between
food intake and fitness: mechanisms for the evolution
of animal personalities
Stamps (2007) proposed that animal personalities are
relatively consistent over time since risk taking and other
behaviours promoting high food intake rates are driven by
individually consistent intrinsic growth rates. An animalÕs
behavioural foraging potential, composed of traits, such as
activity, exploration, boldness and aggressiveness, is associated with growth rate, given that growth is regulated by the
intake of resources (e.g. Petherick et al. 2002; Ward et al.
2004). As natural selection acts on intrinsic growth rates
(Arendt 1997), adaptive individual differences in behaviours
(e.g. activity, boldness and aggressiveness) might be
explained by interindividual variation in intrinsic growth
capacity and trade-offs between growth and mortality that
differ among individuals, but allow them to achieve equal
fitness (Stamps 2007; Biro & Stamps 2008; also see
Adrianssens & Johnsson 2008). However, this mechanism
for the evolution of personality relies upon pre-existing
genetic differences among individuals in intrinsic growth
rates (or underlying traits) to drive the evolution of different
behavioural types (personalities).
Alternative mechanisms that emphasize links between
behaviour and relatively stable state variables have been
proposed for the evolution of animal personalities. These
mechanisms include asset protection, i.e. trade-offs between
current vs. future reproduction and avoidance of starvation
(Wolf et al. 2007; but see Massol & Crochet 2008), and
positive feedback loops in state-dependent behaviour
(McElreath et al. 2007; Luttbeg & Sih 2010). Recently,
Luttbeg and Sih (2010) showed that negative feedback
mechanisms, such as asset protection and starvation
avoidance eventually lead to convergence of behavioural
types over timescales comparable to an individualÕs lifetime,
and therefore cannot account for the long-term stability
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Idea and Perspective
of personalities. However, long-term stability was achieved
when these negative feedback mechanisms were combined
with a positive feedback mechanism, state-dependent safety
(Luttbeg & Sih 2010). Thus, state-dependent safety, for
example, condition-dependent avoidance of predation – or
as we argue here, parasitism – could favour the development
of stable personalities by maintaining and reinforcing
individual differences that arise from small disparities in
original assets (Luttbeg & Sih 2010). Importantly, models by
Stamps (2007; also see Biro & Stamps 2008) and Luttbeg
and Sih (2010) are not mutually exclusive and yield the same
prediction: high life-history productivity and bold behaviours will be coupled. Here, we discuss how parasitism can
change the predictions of productivity ⁄ mortality models
(Stamps 2007; Biro & Stamps 2008) and generate positive
feedback loops between host immune function and behaviour, analogous to those generated by condition-dependent
avoidance of predation (Luttbeg & Sih 2010). We first
separate the effects of parasite exposure on personality
variation from parasite-induced selection on personality
traits, and then discuss how state-dependent safety, generated by the hostÕs immune function, affects the costs of
acquiring parasites through certain behavioural styles.
Parasites and pathogens as selective agents
In general, parasites and pathogens are just as important as
predators in determining individualsÕ fitness (e.g. Raffel et al.
2008; Schmid-Hempel 2009). Even though many parasites
do not directly kill their hosts, they often weaken or
manipulate their hosts, so that the hosts become more
susceptible to predation (e.g. Milinski 1990; Seppälä &
Jokela 2008). Moreover, parasites can cause low fecundity,
sterility or low reproductive rates due to poor success in
intraspecific or interspecific competition (e.g. Kavaliers et al.
2000; Barber et al. 2004; Newey & Thirgood 2004). They
may also decrease the hostÕs mating success due to the
opposite sexÕs avoidance of parasitized mates (Hamilton &
Zuk 1982).
Direct effects of parasitism on host behaviour are diverse
and relatively well known. Exploitation of hosts by parasites
can affect the hostsÕ feeding rates, sociability, migration and
success in sexual selection (Lozano 1991; Hart 1997; Jog &
Watve 2005; Fleurance et al. 2007). In addition, parasites
manipulate hosts to increase their own transmission rates,
often by increasing the hostsÕ risk of predation (Seppälä &
Jokela 2008) or the hostsÕ aggressiveness (as in rabies;
Niezgoda et al. 2002). Therefore, parasites may, by directly
altering host behaviour, create apparent personalities or
behavioural syndromes during the hostÕs life time (e.g. Coats
et al. 2010; see review in Barber and Dingemanse 2010). Our
focus here, however, is on parasite-generated selection
on genotypes. For example, parasite avoidance can be
Idea and Perspective
considered as a behavioural form of parasite resistance that
evolves in response to parasitism. Parasite avoidance is
comprised of behaviours that reduce exposure to parasites,
for example, moving away from particular areas, such as
beddings or nests (Moore 2002; Ezenwa 2004), or removing
macroparasites by grooming or scratching. Population-level
studies have demonstrated that populations under selection
by certain parasites show increased parasite avoidance
behaviour (e.g. Cruz et al. 2008). Notably, parasites (especially microparasites) are more difficult to avoid through
immediate behavioural responses than predators, because
the infectious stages of many parasites cannot be observed.
When parasite exposure is associated with personality
traits, direct and indirect parasite-induced selection for
personality traits may occur. Potential examples of this
phenomenon occur in juvenile pumpkinseed sunfish, in
which parasite fauna differ among individuals along a shy–
bold continuum (Wilson et al. 1993); Siberian chipmunks, in
which non-random distributions of parasites among hosts
result from personality-related differences in space use
(Boyer et al. 2010); and in feral cats, in which higher levels of
lethal feline immunodeficiency virus occur in males with
more aggressive personalities (Natoli et al. 2005). Likewise,
in domestic cats, feline immunodeficiency virus is associated
with aggressiveness, large body size and potentially, earlier
age at first reproduction (Pontier et al. 1998).
Role of host parasite avoidance and resistance
Links between behavioural traits and the cost of parasitism
are necessary for parasitism to affect the evolution of animal
personality. To evaluate the effects of past and current
behaviour on the cost of parasitism, it is important to
consider individual differences in both exposure to parasites
and immune function. These two factors have very different
natures. While exposure to parasites may be a function of
certain behaviours, the cost of that exposure likely varies
between individuals in accordance with their capacity to
resist parasites. In vertebrates, the effectiveness of the
immune system depends on the innate availability of
particular major histocompatability (MHC) alleles and
previous exposure to parasites (Woelfing et al. 2009).
In contrast, invertebrate immunity relies more on intrinsic,
non-specific defences, such as encapsulation and melanization of intruders by the prophenoloxidase-cascade (e.g.
Cerenius & Söderhäll 2004; Lee 2006). In addition, parasite
resistance and tolerance are energetically costly, and involve
trade-offs with other life-history traits (e.g. Zuk & Stoehr
2002; Rantala et al. 2003; Tschirren & Richner 2006).
In turn, the higher is the resource availability, the more
organisms are expected to invest in immune function
(Houston et al. 2007). Therefore, the cost of parasitism will
depend on the intrinsic and condition-dependent qualities
Personalities and parasitism 1451
of an individual and might also reflect an individualÕs
investment in immune defence in earlier phases of life.
Various models for the evolution of personality (e.g.
Luttbeg & Sih 2010) rely upon initial differences in assets
among individuals, even if these are very small. However,
hypotheses relying on stochastic initial differences in assets
or state of individuals do not ultimately explain the adaptive
origin of variation in animal personalities. Here, we provide
an ultimate explanation for adaptive variation in animal
personality by arguing that inherently co-evolutionary and
frequency-dependent host parasite interactions maintain
interindividual variation in immune function and therefore
set different adaptive values for different behavioural styles
under the risk of parasitism. We argue that innate
differences may be reinforced through positive feedback
loops in which high resource-intake rates lead to efficient
immune function. Therefore, the immune system is potentially a generator of variation in initial assets, necessary for
the development of different personalities (Ôbehavioural
typesÕ, Luttbeg & Sih 2010), and of positive feedback loops
that promote and maintain this divergence. Moreover, as
individuals with efficient immune function pay a smaller
cost for parasite exposure than individuals that accumulate
high parasite loads due to inefficient immune function, we
predict, under the positive feedback framework, that
immunologically competent individuals should generally be
more bold and active than less immunocompetent individuals (also see Barber and Dingemanse 2010). We argue that
although individuals with inefficient immune function could
try to compensate for their innately poor immunocompetence by increasing boldness, the compensation is unlikely
to be successful due to frequency-dependent factors or
stochastic events involved in feeding behaviour (see also
discussion in Dall et al. 2004) and the high potential for
extra costs of acquiring more parasites through increased
boldness.
We also argue that direct parasite-induced selection on
certain personality traits is very likely to occur (also see
Barber and Dingemanse 2010). For example, active, social
or group-living individuals encounter parasitized conspecifics more often than do sedentary or solitary individuals,
which can considerably accelerate the transmission of
parasites, particularly horizontally (directly) transmitting
parasites and pathogens (Coté & Poulin 1995; Hart 1997;
Altizer et al. 2003). Increasing the frequency of social
contacts significantly increases parasite spread among
mammals (Altizer et al. 2003; Vicente et al. 2007). This
increased transmission of parasites via social contact is
especially important for infectious diseases, such as influenza or sexually transmitted diseases (e.g. Smith & Dobson
1992; Mosure et al. 1996; Altizer et al. 2003). Indeed,
Schaller & Murray (2008) recently proposed that infectious
diseases can impose strong selection on human personality
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1452 R. Kortet, A. V. Hedrick and A. Vainikka
traits, such as sociosexuality, extraversion and openness to
experience.
Another key factor determining the risk of parasitism
(reviewed in Altizer et al. 2003) is dominance status, which is
usually associated with aggressiveness as well as activity and
boldness (e.g. Kortet & Hedrick 2007). Dominance status
affects both parasite encounter rates and immune function.
Dominant individuals typically have better access to food
resources than subordinate individuals (e.g. Stahl et al.
2001). Although this may increase the risk of acquiring
indirectly transmitted parasites along with food, enhanced
resource intake often improves condition-dependent
immune function. Thus, improved immune function may
compensate all or some of the negative effects of foodborne parasitism (Møller 1997). Dominant individuals often
have stronger immune defence, for example, in field crickets
(Rantala & Kortet 2004) and drumming wolf spiders
(Ahtiainen et al. 2006). In social species, high dominance
status can increase grooming behaviour received from other
individuals, which may decrease the cost of ectoparasitism
(Foster et al. 2010). Dominance status can also affect
endocrine–immunity interactions by affecting the levels
of immunosuppressive androgens and stress hormones
(Hillgarth & Wingfield 1997). For example, subordination
stress in low-ranking fish can increase the risk of parasitism
via stress-induced immunosuppression favouring dominant
individuals (Conte 2004). Similarly, in some mammals,
subordination stress in low-ranking individuals causes
immunosuppression (Sapolsky 2005). In contrast, sex
hormones that promote aggression but induce immunosuppression can indirectly increase the cost of parasitism for
dominant individuals in a number of species (Hillgarth &
Wingfield 1997; Easterbrook et al. 2007). Moreover, in some
animals including cats and wild rats, dominant individuals
have a higher, behaviourally mediated risk of parasitism
through injuries from aggressive encounters (Glass et al.
1988; Pontier et al. 1998; Natoli et al. 2005; Easterbrook
et al. 2007).
In some cases, parasitism strengthens the behaviourally
mediated (via bold, active, aggressive behaviours) trade-off
between productivity and mortality compared to the tradeoff induced by predation alone. For example, aggressive,
dominant rats with a higher risk of parasitism from injury
during fights (Glass et al. 1988) might also incur higher risks
of predation than shy, subordinate rats, because of their
higher activity levels. Here, selection against aggressiveness ⁄
boldness ⁄ activity would be stronger than that predicted by a
predation-only model, possibly promoting the persistence of
shy behavioural types. In contrast, when behavioural traits
such as aggressiveness are associated with a lower risk of
parasitism, as occurs in many species in which dominant
individuals have lower parasitism risks (e.g. Altizer et al.
2003), selection against aggressiveness ⁄ boldness ⁄ activity
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Idea and Perspective
would be weaker than that predicted by a predation-only
model.
The examples above illustrate the fact that associations
between parasite exposure and particular behaviours are
probably multifaceted and should often be considered
species- and context-specific. Ultimate mechanisms that
may influence the impact of parasites on the evolution of
personality include the host–parasite populationsÕ environment and their preceding co-evolutionary history. For
example, host social organization and mating system should
influence not only parasite diversity and prevalence, but also
fitness advantages to parasites of different transmission
strategies (Altizer et al. 2003).
Interindividual and intraindividual variation in behaviour
For personalities to be detected in a population, both low
intraindividual and relatively high interindividual variation in
behaviour must be present (Bell 2007; Stamps and Groothuis
2010). Inherently frequency-dependent co-evolutionary
dynamics between hosts and parasites generate and maintain
genetic variation among hosts (Anderson & May 1982;
Salathé et al. 2007; Woelfing et al. 2009), as parasites, due to
their shorter generation times, usually evolve faster than their
hosts, and impose continuously changing selection pressures
on their hosts. This is probably not the case in predator–prey
co-evolution, as predators usually have longer or similar
generation times compared to prey. Co-evolutionary parasite–host dynamics mean that parasites can contribute to the
maintenance of genetic variation both in initial assets that
favour personality differences, and in direct parasite-induced
selection on personality traits. Thus, parasites impose strong
selection on host immune function and favour maintenance
of variation in several facets of immune defence, including
MHC genes (Anderson & May 1982; Woelfing et al. 2009).
We therefore argue that host parasite co-evolution, which is
ubiquitous in nature, is responsible for intrinsic differences
in host immune function and that these induce initial
differences in individual state (see Luttbeg & Sih 2010).
However, we acknowledge that interindividual variation in
initial assets may also be generated by other mechanisms
including, for example, differences in metabolic rate (Careau
et al. 2009), differences in anti-predator ability, susceptibility
to stress or intrinsic growth rate (Stamps 2007), differences
in parental investment or luck early in life (Luttbeg & Sih
2010).
We argue here that intrinsic differences in host immune
function affect the individual-level cost of parasite exposure.
We argue further that due to the lower cost of parasite
exposure for individuals with a high intrinsic capacity to
resist parasites, condition-dependent improvement of
immune defence is unlikely to override but rather reinforces
initial state differences. Individuals may decrease the cost
Idea and Perspective
Personalities and parasitism 1453
of parasitism whereas hostsÕ parasite resistance is not
affected. In Fig. 1b, PAPs are independent of the risk of
parasitism but increasing PAPs improve parasite resistance
so that the cost of parasitism decreases with increasing level
of PAPs. We aim to explain: (1) the consistency of
individual behaviour, (2) average level of PAPs and (3)
population-level variation in PAPs as a function of the
abovementioned factors. We assume that interindividual
differences are generated and maintained by the mechanisms we have discussed above.
In our example, the risks and costs of predation and
parasitism are additive and independent of host body size.
By this definition, cost of one type imposes a moderate
trade-off between productivity and mortality, and the
maximum cost imposes a strong trade-off. We also assume
that individuals do not use special allocation strategies
between anti-predator and anti-parasite strategies vs. growth
and reproduction, but that once increasing resource-intake
rates, they increase investment in both life-history productivity and safety provided by enhanced immune function
(Houston et al. 2007). We also assume that food intake rates
are independent of population density.
To predict evolution, we make the following simplifying
assumptions about how trade-off strength relates to the
of parasite exposure by investing more resources in parasite
resistance, but only in relation to their intrinsic resistance
capacity. Therefore, we postulate that the stronger is the
selection imposed by parasites, the more likely is low
intraindividual (see section below) and high interindividual
variation in behavioural strategies, linked to the cost of
parasite exposure. We also emphasize that interindividual
variation in behaviours is not random, but adaptive,
particularly with respect to individual constraints set by
the physiological capacity to resist parasites.
A conceptual example adding parasitism to
productivity ⁄ mortality models
We argue that the adaptiveness of personality traits
associated with productivity (hereafter PAPs, i.e. personality
traits that promote fast growth ⁄ high fecundity), which in
some species contribute to active, bold and aggressive
behaviours (Stamps 2007; Biro & Stamps 2008), depend not
only on predation risk, but also on how they affect an
individualÕs parasite exposure (Fig. 1a) and resistance
(Fig. 1b). In our conceptual example (Fig. 1), we assume
two possibilities with varying magnitudes regarding parasitism risk. In Fig. 1a, increasing PAPs per se increase the risk
(b)
Cost of parastism
Trade-off with parasitism, Strong trade-off,
medium consistency
high consistency
Additive trade-off,
medium consistency
Weak trade-off,
low consistency
Trade-off with predation
medium consistency
Cost of predation
Degree of compensation by PAPs
(a)
Directional selection,
high consistency
Strong trade-off,
the highest
consistency
Additive trade-off,
elevated consistency
Moderate trade-off,
medium consistency
Strong trade-off,
high consistency
Cost of predation
Figure 1 Predicted level of personality traits associated with productivity (PAPs) as: (a) a function of the cost of predation and cost of
parasitism, and (b) as a function of the cost of predation and resource-intake-dependent immunity (compensation). The predictions apply
both in evolutionary time at a population level and in ecological time at an individual level given that individuals vary in their initial state with
respect to both parasite resistance and anti-predator ability. (a) We assume that the risks of predation and parasitism are additive and no
compensation of either type of cost occurs. (b) We assume that PAPs mediate compensation of the cost of parasitism. The cost of parasitism
is assumed to be high at the x-axis (when no compensation occurs). At an individual level, the degree of compensation also applies to
differences in the efficiency of immune function. Phenotypically plastic compensation of the cost of predation does not occur in either (a) or
(b). The darker the circle, the more active ⁄ bolder an individual ⁄ individuals should be, and the lighter the circle the less active an
individual ⁄ individuals should be. The greater the diameter of the circle, the stronger is the expected consistency in personality traits, i.e. the
more likely it is that animal personalities may develop ⁄ evolve given that interindividual variation occurs. In contrast to the left lower corner in
(a), in the upper left corner of (b) a high level of interindividual variation in current parasite resistance (from reinforcement of initial
differences through state-dependent positive feedback, see the main text) induces a high level of intraindividual behavioural consistency. Note
that the amount of interindividual variation in PAPs is not demonstrated in the figure, but likely depends on the strength of selection and
variation in individual assets (see the main text).
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1454 R. Kortet, A. V. Hedrick and A. Vainikka
optimal level of PAPs and the population-level variation in
PAPs. If the fitness costs of increasing PAPs increase more
rapidly than the benefits, i.e. the costs are accelerating, for
example because intake-dependent compensation is inefficient against a high risk of parasites, selection is likely
leading to a single evolutionary endpoint (c.f. Hoyle et al.
2008). In contrast, when PAPs increase survival, for
example, by decreasing the cost of parasitism, and the costs
are strongly decreasing, evolution may proceed towards
maximal average levels of activity ⁄ boldness (c.f. Hoyle et al.
2008). However, with more weakly accelerating, linear or
decelerating costs, the evolutionary outcomes are more
difficult to predict but may, at least in non-sexual models,
include a stable polymorphism of different behavioural
types (de Mazancourt & Dieckmann 2004; Hoyle et al.
2008). In this respect, note that Fig. 1 should be interpreted
only as an explanatory example and not as a quantitative
model. Our assumed scenarios differ in that Fig. 1a assumes
no feedback – host resistance varies, but not in response to
PAPs, whereas Fig. 1b assumes a positive feedback, where
PAPs bring in the energy that drives an increase in
host resistance. Host parasite interactions are inherently
frequency-dependent (Anderson & May 1982), and negative
frequency-dependent selection pressure arising from the
host population itself or from parasites could complicate
our simple predictions.
Personality and parasite exposure
According to our conceptual example, the trade-off between
PAPs and mortality in the productivity-mortality model will
be strengthened when parasites are acquired through PAPs
and there is no resource-dependent improvement of parasite
resistance (Fig. 1a, along y-axis). The stronger the trade-off
is, the more consistently an individual should follow the
behavioural trajectory set by its initial and current assets and
the more likely it is that animal personalities will develop
(Fig. 1a). This is explained by the increasing cost of
deviating from an optimal behavioural trajectory that is set
by initial and current assets. For example, an individual with
inefficient immune function will do poorly by behaving in a
way that increases parasite exposure, if a behavioural way to
avoid parasites exists, and similarly, an individual with
efficient immune function loses potential benefits by
unnecessarily avoiding parasites. The same is true with
predators if individuals differ in qualities that affect their
likelihood of being killed by a predator. When the risks of
predation and parasitism are close to zero, we would expect
to see a maximum level of PAPs, but intraindividual
variation in PAPs may exceed that of interindividual
variation, and personalities may not develop (Fig. 1a, lower
left corner). The situation is even more pronounced if
parasites are not acquired through PAPs, but through
behaviours that are coupled with low productivity rates (e.g.
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Idea and Perspective
shy and sedentary behaviour). In such cases, parasites will
decrease the cost of boldness ⁄ high activity and weaken the
trade-off further (not shown in the figure).
Thus, when we abandon the potential for conditiondependent variation in parasite resistance, and the costs of
parasitism and predation are additive, animal personalities
most likely develop in environments with high risks of both
parasites and predators (Fig. 1a, upper right corner), as both
predators and parasites can affect the adaptiveness of
behaviours in relation to intrinsic variation in individual
state. This occurs because we assume that interindividual
variation in initial assets is constant along the lower left to
upper right diagonal (Fig. 1a), and consistency in individual
behaviour increases as the cost increases of deviating from
the optimal trajectory set by initial assets. However, in
nature the likelihood of detecting personalities in a
population depends also on the amount of interindividual
variation in personality traits. This is set by variation in
individual assets determining how tightly individuals follow
the same behavioural trajectory (see also Bell 2007).
Simple predictions from Fig. 1a are that: (1) when the
cost of parasitism and risk of predation increase, the
expected average level of PAPs (e.g. activity ⁄ boldness)
decreases; and with lower costs of parasites and lower risk
of predation, the expected level of PAPs increases. We also
predict that (2) when the trade-off between PAPs and
fitness costs is strong, it is more likely that individual
behaviour will match the assets generated by immune
function (or other physiological factors), and consequently,
it is more likely that animal personalities will develop or
evolve within a population. In this scenario, personality
variation is based wholly on initial rank order state
differences, which may remain even when individual state
feeds back positively to individual state (see below).
Personality and the compensation of parasitism
In Fig. 1b, we assume that high levels of PAPs increase the
efficiency of immune function through enhanced food
intake rates and thus generate safety and decrease the
strength of the trade-off between PAPs and fitness costs.
We argue that the stronger is the selection imposed by
parasites, the more likely it is that low intraindividual and
high interindividual variation in behavioural strategies,
linked to the cost of parasite exposure, will be maintained
(Fig. 1b). Consequently, animal personalities will most likely
develop in a situation where immune defence is efficient at
decreasing the cost of parasite exposure and when predation
risk adds to the cost of deviating from the individually
optimal behavioural trajectory set by initial and current
assets (Fig. 1b, upper right corner).
The safety generated by high levels of PAPs decreases the
fitness cost of PAPs and therefore favours higher levels of
PAPs than would be expected by the non-compensatory
Idea and Perspective
predation cost model only. This leads to the prediction that
individuals with efficient immune function should show
higher levels of PAPs than individuals with less efficient
immune function (Fig. 1b). Similarly, if individuals can
decrease the cost of predation, for example, by growing
quickly to a large (safe) size, individuals are expected to
show higher levels of PAPs than in situations where PAPs
only increase the cost of predation (not shown in the
figures). If there is full compensation of increased parasite
exposure by condition-dependent improvement of immune
defence (Fig. 1b, upper line), the productivity-mortality
trade-off in predation-only models (Stamps 2007; Biro &
Stamps 2008) will not change except for the fact that asset
differences generated by immune function may still contribute to individual consistency of behaviour.
Predictions based on Fig. 1b are that: (1) when increasing
levels of PAPs promote compensation of the cost of
parasites more than they increase the cost of predation, the
expected level of PAPs should increase (in individuals or
over evolutionary time) and (2) when increasing levels of
PAPs increase the cost of predation more than they provide
compensation for parasites, the expected level of PAPs
should decrease (in individuals or over evolutionary time).
Therefore, the maximum level of PAPs (e.g. maximally
active and bold behaviour) is expected when PAPs reduce
the cost of parasitism and there are no predators (as in
Fig. 1b, or when anti-predator strategies are positively
dependent on PAPs).
PREDICTIONS AND CONCLUSION
Our analysis yields predictions that are readily testable. First,
an empiricist could test whether individuals with efficient
immune function are bolder, more active or explore more
than individuals with less efficient immune function and
whether this relationship is genetically determined. This
prediction arises from the claim that intrinsically immunocompetent individuals suffer a small cost of acquiring
parasites along with food, whereas all individuals can
improve their immune function and parasite tolerance by
acquiring more resources (e.g. Houston et al. 2007). The
prediction should hold for a wide continuum of taxa and it
does not separate intrinsic immunity from conditiondependent immunity, as according to Luttbeg and SihÕs
(2010) positive-feedback model with state-dependent safety,
the positive correlation between boldness and immune
efficiency is reinforced over time. If resource-intakedependent improvement of immune function fully compensates for increased parasite exposure, bolder individuals
should have lower parasite loads. If the compensation is not
efficient enough, they should have higher parasite loads.
Note that if the cost of higher tolerance of parasites requires
higher activity, positive coupling between boldness and
Personalities and parasitism 1455
resource acquisition is still likely to be generated (Andrew
Sih, personal communication). Second, comparative studies
could reveal whether species or populations living in
environments with high predation and parasitism risk more
often show personalities than species or populations living
in low predation and parasitism areas (c.f. Dingemanse et al.
2007). We predict that high risks of predation or parasitism
favour high levels of boldness, when compensation of
predation and parasitism induced fitness costs is efficient,
but low levels of boldness, when the animals have little or
no means of compensating for the high costs of predation
and parasitism. Third, comparative studies or studies using
selected lines (e.g. selected for increased and decreased
immune function) could reveal whether abundant but nonvirulent parasites, against which the host displays conditiondependent parasite resistance, select for higher boldness or
stronger behavioural consistency under constant risk of
predation than virulent parasites that cannot be compensated for by foraging more.
We predict that predation-associated costs will dominate
the evolution of personalities in systems where the cost of
parasitism is not clearly associated with host immune
function. Similar patterns will occur when host immune
functions are inefficient at reducing the costs of parasitism.
However, as some anti-predator strategies, including
behavioural traits, are also condition-dependent (e.g. Petterson & Brönmark 1999; Skajaa et al. 2004), we predict that
fitness compensation through PAPs (e.g. Ôstate-dependent
safetyÕ; Luttbeg & Sih 2010) also occurs in predation-driven
systems, and suggest that the consequences of this
mechanism for the maintenance of variation in animal
personalities should be evaluated further using the foundation laid by Luttbeg and Sih (2010). Most importantly, we
argue that parasites maintain variation in personality traits by
maintaining variation in immune function through host
parasite co-evolution. This process is inherently frequencydependent and therefore unquestionably generates variation
(Anderson & May 1982). How frequency-dependent factors
affect interindividual and intraindividual variation in PAPs,
depending on population-level feedback mechanisms such
as density-dependent food availability and probability of
aggressive encounters, is less clear. Whereas maximum
activity and low consistency is the apparent outcome in our
simplified scenarios with zero costs, frequency- and densitydependent factors will probably come into play in real
situations, and maximal aggressiveness, for example, would
be an evolutionarily stable strategy in a predator and parasite
free environment only if an individual was short of food (see
e.g. Houston & McNamara 1988). On the other hand, certain
frequency-dependent behaviours are capable of maintaining
rank order differences in individual state and do not affect
life-history trajectories induced by differences in initial state
(Dall et al. 2004). In any case, the effect of factors such as
2010 Blackwell Publishing Ltd/CNRS
1456 R. Kortet, A. V. Hedrick and A. Vainikka
density-dependent availability of food and developmental
and physiological constraints in food intake rates and
growth rates should be taken into account to fully
understand the effects of frequency dependence. Thus, a
more detailed formal modelling approach is needed.
To date there are very few empirical tests of the ideas
presented here. However, Kortet et al. found a positive
correlation in field crickets between boldness and lytic
activity, a measure of the cricketsÕ defence against bacterial
parasites (Kortet et al. 2007). Correlations such as this are
difficult to interpret without knowing the relationships
between behaviour, parasitism and the condition dependence of studied measures of immune function. In this
particular example (Kortet et al. 2007), the correlation could
suggest that bold behaviour facilitates a high resourceacquisition rate, which facilitates an aspect of strong
immune function. Alternatively, innately resistant individuals may be better able to cope with the risk of acquiring
parasites with food, and for this reason might behave more
actively, aggressively or boldly than their less resistant
conspecifics (see also López et al. 2005). Indeed, it may be
possible that both of these two causal mechanisms are at
work. Tests of immunity–personality interactions are warranted and the results will help to further develop the ideas
presented here. For example, positive feedback loops
between PAPs and immune functions, particularly during
ontogeny, should generate divergent personalities which
may appear heritable in quantitative genetic analyses due to
the underlying inheritance of immune components.
In conclusion, we assert that parasites and pathogens can
strongly affect the costs and benefits of many personality
traits. We also propose that initial variation in individual
assets can be generated by host parasite co-evolution, and
that the consequently arising differences in immunity can
induce positive feedback loops between fitness and behaviours promoting high food intake rates, favouring different,
individually consistent behaviours (personality traits) over
long periods of time. Our work adds to the premises that
trade-offs between behaviourally mediated productivity and
mortality (Stamps 2007; Biro & Stamps 2008) and positive
feedback loops between state-dependent safety and behaviour (Luttbeg & Sih 2010) can guide the evolution of animal
personalities.
ACKNOWLEDGEMENTS
This research has been supported by the Academy of Finland
(project 127398), the National Science Foundation (IOS0716332) and by a grant from the Emil Aaltonen foundation.
We thank Andy Sih, Judy Stamps and Kelly Smith for very
helpful comments, and Iain Barber and Niels Dingemanse,
as well as Barney Luttbeg and Andy Sih, for providing us
with pre-publication copies of their manuscripts.
2010 Blackwell Publishing Ltd/CNRS
Idea and Perspective
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Editor, Andrew Sih
Manuscript received 24 June 2010
First decision made 5 August 2010
Manuscript accepted 11 September 2010